RESEARCH PROJECTS:

SENSORY SIGNALS OF LOAD IN FREELY WALKING ANIMALS

Summary: Our research is studying a problem that is basic to understanding the control of posture and walking: How are forces generated by the legs adjusted to provide support of the body weight? These types of adjustments are made normally during walking and also occur in traversing uneven terrains, in carrying objects or when a leg loses footing and slips. To adapt to changing loads, the nervous system modifies the magnitude and timing of contractions of leg muscles.  Sense organs located in the legs are thought to provide information needed for these adaptive modifications.   However, it is not clear how these sensory receptors specifically signal the effects of body load in a standing or walking animal.  This problem is important in understanding the control of posture and locomotion in both vertebrate and invertebrate animals and in the design of prosthetic devices and walking robots.  To gain insight into this process, we have performed experiments in which the activities of receptors that can encode forces in the legs are recorded in freely behaving animals while loading is experimentally changed. 

Specifically, our experiments have recorded the activities of campaniform sensilla, sense organs that monitor forces in the cockroach leg, when body load is altered in animals that are freely standing or walking.   In our studies, the weight supported by the legs is increased by attaching small neodymium magnets to the body (thorax).   The mass and number of the magnets can be adjusted so that the body weight is tonically increased by a known amount.  The load upon the legs can also be changed dynamically by activating a coil placed below the walking arena.  Currents applied to the coil attract or repel the magnet, producing rapid increases or decreases in the effective body weight.   The effects of changes in load are also monitored by video taping animals (to measure body position and movement), and by recording activities of leg muscles.

1) SERIAL HOMOLOGY AND LOAD COMPENSATION: COMMON SENSORY-MOTOR MECHANISMS IN COCKROACH FRONT AND HINDLEGS. (Click to See Full Presentation)

Forelimbs can function both as legs and arms in many animals, including insects. This diversity of use complicates analysis of neuronal control of posture and locomotion. As part of a project examining sensory encoding of load, we are studying anatomical and sensory-motor mechanisms in cockroach front legs that mediate support of body weight. In contrast to the well-studied hindlegs, front legs are much smaller and attached to the body by joints with considerable freedom of movement. However, maps of sense organs, intrinsic muscles and elastic ligaments show clear homologies. We have recorded activities of tibial campaniform sensilla, sensory receptors that encode forces in the limb via exoskeletal strains, and muscles of the front leg while body load is changed in freely standing animals. Effective body weight is varied via magnets attached to the thorax and currents applied to a coil below the substrate. Load increments produce vigorous firing of proximal tibial campaniform sensilla and the trochanteral extensor muscle in both front and hindlegs. The front leg trochanteral extensor motoneuron (Ds) shows tonic coupling to the level of load (evidenced in tests using very slow sine wave currents), consistent with a more vertical orientation of its plane of action. The muscle also has a broad tendon (apodeme), comparable in size to that found in the hindleg, suggesting a common function as a serial compliant element. Our studies suggest that, despite apparent wide dissimilarity in size and use, serially homologous sensory-motor elements supporting body load are present in the front leg, amid modifications that provide flexibility for its functions as a manipulandum or arm-like structure. Support Contributed By: NSF Grant IBN-0235997

2) TUNING POSTURE AND LOCOMOTION TO BODY LOAD: COMMON MECHANISMS OF LOAD SENSING AND DISCRETE CHANGES IN MOTOR ACTIVITIES IN WALKING IN COCKROACHES. (Click to See Full Presentation) 

Forces needed to support body weight are generated by the concerted action of legs in stance. These forces continuously vary in individual limbs when walking. We are studying the effects of changes in body load that are imposed via magnets attached to the thorax of freely moving cockroaches. Discharges of tibial campaniform sensilla, receptors that encode forces in the limb via exoskeletal strains, are monitored neurographically. Activities of leg muscles are recorded and animals are videotaped. Data are now being obtained in each of the serially homologous legs. Our results to date indicate that there are common mechanisms for support of body load in all legs. In posture, load increments can elicit vigorous firing of proximal sensilla and the trochanteral extensor muscle of the front, middle or hindlegs. This pattern is consistent with an interjoint reflex that can be elicited by stimulation of proximal receptors in each leg. During walking, proximal sensilla in all limbs are active in stance while distal receptors discharge prior to swing. Our recent studies have shown that sensory activities in the front and middle legs persist in walking with body weight supported over an oiled glass plate. Thus, all groups of sensilla are apparently responsive to both load and muscle forces. In walking of freely moving animals, tonic increases in body load (approximately 30% body weight) produce slower walking rates but with similar temporal parameters within the step cycle. These loads elicit specific changes in extensor activities in the front and middle legs. Extensor bursts are initiated during swing and continue through most of stance but loads produce increased firing only after foot placement. These data suggest that activities of muscles providing support in slow walking are tuned by mechanisms that occur during the stance phase, when discharges of receptors monitoring forces are maximal.

3) EFFECTS OF INCREASED BODY LOAD IN COCKROACH WALKING AND RUNNING  (Click to See Full Presentation)

Compensation for load is necessary for posture and adaptive locomotion but may be limited during rapid movements. We are studying mechanisms underlying support of body load in cockroaches. Body weight is increased in freely moving animals by small magnets attached to the thorax and varied by a coil below the substrate. Our previous studies showed that 1) increases in body load in freely standing cockroaches can produce activation of leg receptors that detect forces (campaniform sensilla) and the trochanteral extensor muscle in all legs and 2) tonic increases in load enhance sensory and motor activities during the stance phase when animals walk slowly. We are currently examining the effects of 1) tonic load increases in rapid walking and 2) sudden load changes applied during stance. Animals are videotaped at high speed to measure kinematic parameters and body position. Sensory and motor activities are recorded neurographically. Animals with tonically increased load that are walking rapidly show substantial decreases and greater variability in height above the substrate than is seen in slow walking. Our data to date indicate that extensor firing frequencies are less adapted to load increases at higher walking rates. These effects are correlated with the rate of walking: cockroaches can change from poor (low and variable body height) to adequate compensation (increased height, decreased fluctuations) within single sequences if the walking rate is slowed. Animals also readily adapt to sudden load increases that are applied during slow walking and show transient decreases in body height and modulation of motoneuron firing frequencies. We are currently analyzing sensory and motor discharges that occur during perturbations at different walking rates. However, our results to date indicate that cockroaches can compensate for body load when walking slowly but do not adapt to load increases when running. These findings are consistent with the idea that running is a centrally determined program which is effective in escape but poorly modifiable by changes in load.

4) DISCRETE SENSORY SIGNALS OF LOAD DECREASES IN THE LEGS OF FREELY MOVING COCKROACHES  (Click to See Full Presentation)

Decreases in load are important cues in the control of posture and walking, but the specific receptors that signal leg unloading have been identified in only a few systems. We recorded activities of the tibial campaniform sensilla, receptors that monitor forces as strains in the exoskeleton, in freely moving cockroaches. The effective body load was changed via magnets attached to the thorax and currents applied to a coil below the substrate. Body position was monitored by high speed video recording. The tibial sensilla are organized into proximal and distal subgroups. Recent studies have demonstrated that the anatomical arrangement and number of receptors is similar in all legs. The proximal and distal sensilla showed differential responses to changes in load in freely standing animals. Tests in which loading was suddenly increased produced short latency firing of proximal sensilla of the middle leg, while imposed forces that decreased body load elicited bursts from the distal sensilla. In both increases and decreases in load, sensory discharges more closely approximated the time of peak velocity of body movement than the maximum change in body position. Tests in which forces were applied for longer durations showed that the proximal sensilla discharged tonically and reflected the magnitude of load increases, while the distal sensilla typically responded only phasically to sustained unloading. Distal sensilla also had a higher threshold than proximal receptors, and the threshold depended upon both the rate and amplitude of unloading. Thus, these studies strongly suggest that 1) small variations in load are signaled by modulation of firing of proximal sensilla, which can reflexly excite extensor motoneurons to provide support of body load; 2) large or rapid load decreases specifically excite distal sensilla in freely standing animals, which can inhibit extensor firing. These decreases in load should occur prior to leg lifting in swing or when a leg slips and loses contact with the substrate. We are presently recording the activities of leg muscles that support body load to examine how sensory cues of decreased load are integrated into motor outputs. Although specific sense organs that detect unloading have not been identified in vertebrates, similar functions could be fulfilled by receptors of the feet in signaling load decreases in posture and locomotion. 

5) DETECTING LOAD IN PEDAL EXTREMITIES: STRUCTURE AND RESPONSES OF SENSE ORGANS THAT ENCODE FORCES IN THE TARSI OF COCKROACHES (Click to See Full Presentation)

Our research is characterizing how forces are detected in the legs of cockroaches. Recent studies in a variety of animals have shown that sensory inputs from the feet can provide important information in the control of posture and walking and may also aid in adapting motor responses to variations in the substrate. To characterize information provided by sense organs of the feet and compare it with responses of receptors detecting forces in the proximal leg, we are recording sensory activities in the tarsus by wires placed in the first tarsal segment. Units are confirmed as sensory by recordings taken simultaneously in the tibia, which show 1:1 spiking at a delay due to centrifugal conduction. Forces are applied to the tarsus in restrained preparations using a probe mounted to a piezoelectric crystal. Recordings regularly show a single unit with a particularly large spike that responds to forced extension of the joint between the fourth and fifth tarsal segments (Ta45). The frequency of afferent firing encodes both the rate and amplitude of applied force. Control experiments strongly suggest that this activity is derived from a campaniform sensillum located on the distal condyle of the fourth tarsal segment (Ta4): ablation of the tarsus distal to the joint does not eliminate the sensory discharge while ablation of the cuticle of Ta4 eliminates all responses of equivalent amplitude. In addition, small indentations of the tarsus in the region of the cuticular cap of the sensillum produce action potentials of amplitude equivalent to that seen in bending tests. We have also studied the structure of the distal tarsus by histological section and confocal microscopy and characterized movements of the joint by high speed video imaging. These studies suggest that the Ta45 joint serves as a fulcrum for movements of the distal tarsus. However, forces are transmitted through the joint only when the claws and arolium are engaged with the substrate by the action of the pretarsal depressor (retractor unguis) muscle. We are planning to study responses of tarsal sense organs in freely standing animals during tests in which body load is changed by attaching a magnet to the dorsum of the animal and applying currents to a coil below the arena. Preliminary tests show that decreases in body load can produce firing of a large unit when animals can grasp the substrate and that this discharge is eliminated by ablation of cuticle at the Ta45 joint. Sensory inputs from the tarsi may, therefore, provide information about the forces exerted by the leg within the frame of reference of the foot and potentially aid in adapting motor responses to properties of the substrate. Support Contributed by: NSF Grant IBN-0235997

Copyright 2006 Joan C. Edwards School of Medicine. All rights reserved.